Twist1 and snail link hedgehog signaling to tumor-initiating cell-like properties and acquired chemoresistance independently of ABC transporters

Stem Cells

Volumn 33, Issue 4, 2015, Pages 1063-1074

  Kong, Ying ^a   Peng, Yuanqiu ^a   Liu, Yuan ^a   Xin, Hong ^a   Zhan, Xia ^a   Tan, Wenfu ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

Acquired chemoresistance; Hedgehog; Snail; Tumor initiating cell like properties; Twist1

Indexed keywords

ABC TRANSPORTER; DOCETAXEL; DOXORUBICIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GLI1; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR TWIST1; UNCLASSIFIED DRUG; VINCRISTINE; ANTINEOPLASTIC AGENT; NUCLEAR PROTEIN; SNAIL FAMILY TRANSCRIPTION FACTORS; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR TWIST; TWIST1 PROTEIN, HUMAN;

ARTICLE; CANCER CELL LINE; CANCER RESISTANCE; CANCER STEM CELL; CELL DIFFERENTIATION; CELL RENEWAL; CONTROLLED STUDY; FEMALE; HEDGEHOG SIGNALING PATHWAY; HUMAN; HUMAN CELL; IN VIVO STUDY; K562 CELL LINE; KB CANCER CELL; LIMB DEVELOPMENT; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION SITE; 3T3 CELL LINE; ANIMAL; BIOSYNTHESIS; DRUG EFFECTS; DRUG RESISTANCE; METABOLISM; MOUSE; NONOBESE DIABETIC MOUSE; PHYSIOLOGY; SCID MOUSE; TUMOR CELL LINE;

ERINACEIDAE; GASTROPODA;

ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; ATP-BINDING CASSETTE TRANSPORTERS; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; HEDGEHOG PROTEINS; HUMANS; K562 CELLS; MICE; MICE, INBRED NOD; MICE, SCID; NEOPLASTIC STEM CELLS; NIH 3T3 CELLS; NUCLEAR PROTEINS; TRANSCRIPTION FACTORS; TWIST TRANSCRIPTION FACTOR; VINCRISTINE;

EID: 84925661239     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.1955     Document Type: Article

References (39)

1. Lage H,. An overview of cancer multidrug resistance: A still unsolved problem. Cell Mol Life Sci 2008; 65: 3145-3167.
2. Reya T, Morrison SJ, Clarke MF, et al. Stem cells, cancer, and cancer stem cells. Nature 2001; 414: 105-111.
3. Clarke MF, Dick JE, Dirks PB, et al. Cancer stem cells-Perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res 2006; 66: 9339-9344.
4. Mani SA, Guo W, Liao MJ, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008; 133: 704-715.
5. Polyak K, Weinberg RA,. Transitions between epithelial and mesenchymal states: Acquisition of malignant and stem cell traits. Nat Rev Cancer 2009; 9: 265-273.
6. Dean M, Fojo T, Bates S,. Tumour stem cells and drug resistance. Nat Rev Cancer 2005; 5: 275-284.
7. Fillmore CM, Kuperwasser C,. Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy. Breast Cancer Res 2008; 10: R25.
8. Bertolini G, Roz L, Perego P, et al. Highly tumorigenic lung cancer CD133+ cells display stem-like features and are spared by cisplatin treatment. Proc Natl Acad Sci USA 2009; 106: 16281-16286.
9. Creighton CJ, Li X, Landis M, et al. Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc Natl Acad Sci USA 2009; 106: 13820-13825.
10. Calcagno AM, Salcido CD, Gillet JP, et al. Prolonged drug selection of breast cancer cells and enrichment of cancer stem cell characteristics. J Natl Cancer Inst 2010; 102: 1637-1652.
11. Beachy PA, Karhadkar SS, Berman DM,. Tissue repair and stem cell renewal in carcinogenesis. Nature 2004; 432: 324-331.
12. Stecca B, Ruiz IAA,. Context-dependent regulation of the GLI code in cancer by HEDGEHOG and non-HEDGEHOG signals. J Mol Cell Biol 2010; 2: 84-95.
13. Scales SJ, de Sauvage FJ,. Mechanisms of Hedgehog pathway activation in cancer and implications for therapy. Trends Pharmacol Sci 2009; 30: 303-312.
14. Zhan X, Wang J, Liu Y, et al. GPCR-like signaling mediated by smoothened contributes to acquired chemoresistance through activating Gli. Mol Cancer 2014; 13: 4.
15. Domingo-Domenech J, Vidal SJ, Rodriguez-Bravo V, et al. Suppression of acquired docetaxel resistance in prostate cancer through depletion of notch- and hedgehog-dependent tumor-initiating cells. Cancer Cell 2012; 22: 373-388.
16. Park KS, Martelotto LG, Peifer M, et al. A crucial requirement for Hedgehog signaling in small cell lung cancer. Nat Med 2011; 17: 1504-1508.
17. Varnat F, Duquet A, Malerba M, et al. Human colon cancer epithelial cells harbour active HEDGEHOG-GLI signalling that is essential for tumour growth, recurrence, metastasis and stem cell survival and expansion. EMBO Mol Med 2009; 1: 338-351.
18. Sims-Mourtada J, Izzo JG, Ajani J, et al. Sonic Hedgehog promotes multiple drug resistance by regulation of drug transport. Oncogene 2007; 26: 5674-5679.
19. Queiroz KC, Ruela-de-Sousa RR, Fuhler GM, et al. Hedgehog signaling maintains chemoresistance in myeloid leukemic cells. Oncogene 2010; 29: 6314-6322.
20. Singh RR, Kunkalla K, Qu C, et al. ABCG2 is a direct transcriptional target of hedgehog signaling and involved in stroma-induced drug tolerance in diffuse large B-cell lymphoma. Oncogene 2011; 30: 4874-4886.
21. Zhang Y, Laterra J, Pomper MG,. Hedgehog pathway inhibitor HhAntag691 is a potent inhibitor of ABCG2/BCRP and ABCB1/Pgp. Neoplasia 2009; 11: 96-101.
22. Xin H, Kong Y, Jiang X, et al. Multi-drug-resistant cells enriched from chronic myeloid leukemia cells by Doxorubicin possess tumor-initiating-cell properties. J Pharmacol Sci 2013; 122: 299-304.
23. Sasaki H, Nishizaki Y, Hui C, et al. Regulation of Gli2 and Gli3 activities by an amino-terminal repression domain: Implication of Gli2 and Gli3 as primary mediators of Shh signaling. Development 1999; 126: 3915-3924.
24. Chen JK, Taipale J, Cooper MK, et al. Inhibition of Hedgehog signaling by direct binding of cyclopamine to Smoothened. Genes Dev 2002; 16: 2743-2748.
25. Zhan X, Feng X, Kong Y, et al. JNK signaling maintains the mesenchymal properties of multi-drug resistant human epidermoid carcinoma KB cells through snail and twist1. BMC Cancer 2013; 13: 180.
26. Mosmann T,. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J Immunol Methods 1983; 65: 55-63.
27. Dalerba P, Cho RW, Clarke MF,. Cancer stem cells: Models and concepts. Annu Rev Med 2007; 58: 267-284.
28. Lauth M, Bergstrom A, Shimokawa T, et al. Inhibition of GLI-mediated transcription and tumor cell growth by small-molecule antagonists. Proc Natl Acad Sci USA 2007; 104: 8455-8460.
29. Li X, Deng W, Nail CD, et al. Snail induction is an early response to Gli1 that determines the efficiency of epithelial transformation. Oncogene 2006; 25: 609-621.
30. Kinzler KW, Vogelstein B,. The GLI gene encodes a nuclear protein which binds specific sequences in the human genome. Mol Cell Biol 1990; 10: 634-642.
31. Wang SM, Coljee VW, Pignolo RJ, et al. Cloning of the human twist gene: Its expression is retained in adult mesodermally-derived tissues. Gene 1997; 187: 83-92.
32. Ohkuma M, Funato N, Higashihori N, et al. Unique CCT repeats mediate transcription of the TWIST1 gene in mesenchymal cell lines. Biochem Biophys Res Commun 2007; 352: 925-931.
33. Chen JK, Taipale J, Young KE, et al. Small molecule modulation of Smoothened activity. Proc Natl Acad Sci USA 2002; 99: 14071-14076.
34. Xie J, Murone M, Luoh SM, et al. Activating smoothened mutations in sporadic basal-cell carcinoma. Nature 1998; 391: 90-92.
35. Gottesman MM, Fojo T, Bates SE,. Multidrug resistance in cancer: Role of ATP-dependent transporters. Nat Rev Cancer 2002; 2: 48-58.
36. Redmond KM, Wilson TR, Johnston PG, et al. Resistance mechanisms to cancer chemotherapy. Front Biosci 2008; 13: 5138-5154.
37. Krawchuk D, Weiner SJ, Chen YT, et al. Twist1 activity thresholds define multiple functions in limb development. Dev Biol 2010; 347: 133-146.
38. O'Rourke MP, Soo K, Behringer RR, et al. Twist plays an essential role in FGF and SHH signal transduction during mouse limb development. Dev Biol 2002; 248: 143-156.
39. Loebel DA, Hor AC, Bildsoe H, et al. Regionalized Twist1 activity in the forelimb bud drives the morphogenesis of the proximal and preaxial skeleton. Dev Biol 2012; 362: 132-140.